Highly conserved gene order and numerous novel repetitive elements in genomic regions linked to wing pattern variation in Heliconius butterflies

Background: With over 20 parapatric races differing in their warningly colored wing patterns, the butterfly Heliconius erato provides a fascinating example of an adaptive radiation. Together with matching races of its co-mimic Heliconius melpomene, H. erato also represents a textbook case of Müllerian mimicry, a phenomenon where common warning signals are shared amongst noxious organisms. It is of great interest to identify the specific genes that control the mimetic wing patterns of H. erato and H. melpomene. To this end we have undertaken comparative mapping and targeted genomic sequencing in both species. This paper reports on a comparative analysis of genomic sequences linked to color pattern mimicry genes in Heliconius. Results: Scoring AFLP polymorphisms in H. erato broods allowed us to survey loci at approximately 362 kb intervals across the genome. With this strategy we were able to identify markers tightly linked to two color pattern genes: D and Cr, which were then used to screen H. erato BAC libraries in order to identify clones for sequencing. Gene density across 600 kb of BAC sequences appeared relatively low, although the number of predicted open reading frames was typical for an insect. We focused analyses on the D- and Cr-linked H. erato BAC sequences and on the Yb-linked H. melpomene BAC sequence. A comparative analysis between homologous regions of H. erato (Cr-linked BAC) and H. melpomene (Yb-linked BAC) revealed high levels of sequence conservation and microsynteny between the two species. We found that repeated elements constitute 26% and 20% of BAC sequences from H. erato and H. melpomene respectively. The majority of these repetitive sequences appear to be novel, as they showed no significant similarity to any other available insect sequences. We also observed signs of fine scale conservation of gene order between Heliconius and the moth Bombyx mori, suggesting that lepidopteran genome architecture may be conserved over very long evolutionary time scales. Conclusion: Here we have demonstrated the tractability of progressing from a genetic linkage map to genomic sequence data in Heliconius butterflies. We have also shown that fine-scale gene order is highly conserved between distantly related Heliconius species, and also between Heliconius and B. mori. Together, these findings suggest that genome structure in macrolepidoptera might be very conserved, and show that mapping and positional cloning efforts in different lepidopteran species can be reciprocally informative

Wing Patterns in the Mist

Arnaud Martin is with University of California Irvine, Durrell D. Kapan is with University of Hawaii at Manoa, Lawrence E. Gilbert is with UT Austin.The aesthetic appeal of butterfly wing patterns has been costly to their status as a tool of fundamental scientific inquiry. Thus, while mimetic convergence in wing patterns between edible “Batesian” mimics and distasteful models, or between different distasteful “Müllerian” mimics (species that cooperate to educate predators) has long been the subject of genetic analysis [1] and field experiments [2], most biology text books confine mimicry to sections on striking adaptations without applying these examples to broader topics of evolution. Meanwhile, the study of color patterns in animals, often tucked into the same sections of texts, is undergoing a revolution in this age of evo-devo and genomics [3]. Among insect models for studying color pattern, the genus Heliconius is gaining the attention of an ever-widening audience.Biological Sciences, School o

Man Bites Mosquito: Understanding the Contribution of Human Movement to Vector-Borne Disease Dynamics

In metropolitan areas people travel frequently and extensively but often in highly structured commuting patterns. We investigate the role of this type of human movement in the epidemiology of vector-borne pathogens such as dengue. Analysis is based on a metapopulation model where mobile humans connect static mosquito subpopulations. We find that, due to frequency dependent biting, infection incidence in the human and mosquito populations is almost independent of the duration of contact. If the mosquito population is not uniformly distributed between patches the transmission potential of the pathogen at the metapopulation level, as summarized by the basic reproductive number, is determined by the size of the largest subpopulation and reduced by stronger connectivity. Global extinction of the pathogen is less likely when increased human movement enhances the rescue effect but, in contrast to classical theory, it is not minimized at an intermediate level of connectivity. We conclude that hubs and reservoirs of infection can be places people visit frequently but briefly and the relative importance of human and mosquito populations in maintaining the pathogen depends on the distribution of the mosquito population and the variability in human travel patterns. These results offer an insight in to the paradoxical observation of resurgent urban vector-borne disease despite increased investment in vector control and suggest that successful public health intervention may require a dual approach. Prospective studies can be used to identify areas with large mosquito populations that are also visited by a large fraction of the human population. Retrospective studies can be used to map recent movements of infected people, pinpointing the mosquito subpopulation from which they acquired the infection and others to which they may have transmitted it

Divergent natural selection and müllerian mimicry in polymorphic heliconius cydno (Lepidoptera: Nymphalidae)

Natural selection favours bright colours or bold patterns that advertise unpalatability. In a noxious polymorphic species frequency-dependent selection should lead to fixation of the common morph, because rare morphs suffer relatively higher attack rates by naive predators. This generally leads to warning colouration that is monomorphic within species and shared between species (Müllerian mimicry). However, several unpalatable species of Heliconius butterflies (Lepidoptera: Nymphalidae) exhibit polymorphic warning colouration within a population. One possible explanation is that divergent selection may favour different colour-pattern morphs of a single unpalatable species if each matches a different warningly coloured unpalatable Miillerian mimic species (comodels). In this thesis I explore this hypothesis by investigating the genetic basis and fitness consequences of polymorphism for warning-colour pattern within a single species of Heliconius butterfly, H. cydno. In Western Ecuador, H. cydno is polymorphic for colour (yellow versus white), pattern (triangle versus band), and hind-wing band-width. I find that H. cydno's colour-pattern polymorphism has a simple Mendelian genetic basis. Two alleles at a single locus with complete dominance determine colour differences (white alleles dominate over yellow). Pattern differences are slightly more complex: a single locus with three alleles (and complete dominance) or two epistatic diallelic loci can account for the variation. Relative hind-wing band-width may have a polygenic basis. Using the multi-site transplant experiment, I find that divergent selection favours transferred colour-morphs of H. cydno (yellow or white) that resemble their putative Müllerian comodels (H. eleuchia or H. sapho respectively). This provides unique experimental evidence for the benefit of Müllerian mimicry. Divergent selection generated by the two comodels may promote maintenance of the colour-pattern polymorphism in H. cydno. In support of this hypothesis, I found the frequency of yellow H. cydno correlates with the density of their respective comodels (yellow H. eleuchia or white H. sapho) at different locales. H. cydno is also polymorphic for colour and pattern where it occurs in the local absence of comodels. Polymorphism at these sites indicates that gene-flow, reduced selection, or both helps maintain colour-pattern diversity when comodels are absent. My research suggests that Müllerian mimicry can develop between a single species and more than one comodel taxon. In Western Ecuador, two Heliconius species appear to generate divergent selection favouring polymorphism in a third species H. cydno.Science, Faculty ofZoology, Department ofGraduat

Estimates of introgression as a function of pairwise distances

Abstract Background Research over the last 10 years highlights the increasing importance of hybridization between species as a major force structuring the evolution of genomes and potentially providing raw material for adaptation by natural and/or sexual selection. Fueled by research in a few model systems where phenotypic hybrids are easily identified, research into hybridization and introgression (the flow of genes between species) has exploded with the advent of whole-genome sequencing and emerging methods to detect the signature of hybridization at the whole-genome or chromosome level. Amongst these are a general class of methods that utilize patterns of single-nucleotide polymorphisms (SNPs) across a tree as markers of hybridization. These methods have been applied to a variety of genomic systems ranging from butterflies to Neanderthals to detect introgression, however, when employed at a fine genomic scale these methods do not perform well to quantify introgression in small sample windows. Results We introduce a novel method to detect introgression by combining two widely used statistics: pairwise nucleotide diversity d xy and Patterson’s D. The resulting statistic, the distance fraction (d f ), accounts for genetic distance across possible topologies and is designed to simultaneously detect and quantify introgression. We also relate our new method to the recently published f d and incorporate these statistics into the powerful genomics R-package PopGenome, freely available on GitHub (pievos101/PopGenome) and the Comprehensive R Archive Network (CRAN). The supplemental material contains a wide range of simulation studies and a detailed manual how to perform the statistics within the PopGenome framework. Conclusion We present a new distance based statistic d f that avoids the pitfalls of Patterson’s D when applied to small genomic regions and accurately quantifies the fraction of introgression (f) for a wide range of simulation scenarios

Spatially disaggregated disease transmission risk: land cover,land use and risk of dengue transmission on the island of Oahu

Vector-borne diseases persist in transmission systems that usually comprise heterogeneously distributed vectors and hosts leading to a highly heterogeneous case distribution. In this study, we build on principles of classical mathematical epidemiology to investigate spatial heterogeneity of disease risk for vector-borne diseases. Land cover delineates habitat suitability for vectors, and land use determines the spatial distribution of humans. We focus on the risk of exposure for dengue transmission on the Hawaiian island of Oahu, where the vector Aedes albopictus is well established and areas of dense human population exist. In Hawai’i, dengue virus is generally absent, but occasionally flares up when introduced. It is therefore relevant to investigate risk, but difficult to do based on disease incidence data. Based on publicly available data (land cover, land use, census data, surveillance mosquito trapping), we map the spatial distribution of vectors and human hosts and finally overlay them to produce a vector-to-host ratio map. The resulting high-resolution maps indicate a high spatial variability in vector-to-host ratio suggesting that risk of exposure is spatially heterogeneous and varies according to land cover and land us

Parallel Genetic Architecture of Parallel Adaptive Radiations in Mimetic Heliconius Butterflies

It is unknown whether homologous loci underlie the independent and parallel wing pattern radiations of Heliconius butterflies. By comparing the locations of color patterning genes on linkage maps we show that three loci that act similarly in the two radiations are in similar positions on homologous chromosomes

Three natural hybrid zones between parapatric populations of different <i>Heliconius</i> species.

<p>Only a subset of the phenotypic diversity and geographical distribution of the <i>erato</i>, <i>melpomene</i>, and <i>cydno</i> clades is represented. Müllerian mimicry is here illustrated by the convergence in wing patterns of <i>H. melpomene</i> and <i>H. erato</i> on both sides of the Peruvian Andes (yellow and red). <i>H. pachinus</i> and <i>H. cydno</i> are sister species that occasionally hybridize.</p